Evolution of neural induction and dorsal-ventral axis specification: BMP network involvement in annelids

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Many animals have a centralized nervous system (CNS) where neural cells (neurons) are clustered together; an example is the brain and spinal cord of humans. This arrangement of neurons is thought to provide better integration and more sophisticated processing of information, but a thorough understanding of how complex CNSs arose in different animal groups and how these CNSs compare with one another is lacking. This project addresses these questions by examining CNS development in a very understudied group of animals, the annelid worms. Annelids are important for studies of neural development because they have CNSs with thousands of neurons that easily regenerate, unlike other animal CNSs that either do not regenerate well (e.g. humans) or do not have many neurons in their CNS. This project will provide a better understanding of how a complex CNS can form and will develop several techniques as resources for the scientific community, including CRISPR-Cas9 gene editing in the annelid Capitella teleta. This project also will support and train undergraduate and graduate students and a postdoctoral fellow. Finally, the findings and techniques developed in this project will be used to 1) augment undergraduate projects in a developmental biology course, 2) improve current outreach efforts with the Girls, Inc. Eureka summer program to engage local junior-high girls in STEM activities, and 3) develop, implement, and asses a new teaching module for local high school students and teachers that is designed to promote an appreciation of CNS diversity and a better understanding of how animal diversity arose.A key question concerning animal evolution is how CNSs evolved and contributed to organismal diversity. In many animals with a CNS, a whole region of the ectoderm acquires the potential to become neural as part of dorsal-ventral (D-V) axis specification. In vertebrates and insects, Bone Morphogenetic Protein (BMP) signaling plays an important role in both processes. This raises the question of whether or not the last common ancestor of deuterostomes and protostomes had a CNS and whether neural induction was linked to D-V axis specification in this animal. To test these hypotheses, data is needed from additional taxa, especially spiralians, one of two main protostome groups. This project will test these hypotheses by investigating the role of BMP signaling in D-V axis and CNS fate specification in the spiralian annelid Capitella teleta. Project aims are: 1) Determine the degree of conservation of BMP pathway components in C. teleta by characterizing their expression dynamics using in situ hybridization and immunohistochemistry, 2) Assess the ancestral role of BMP signaling through gain- and loss-of-function experiments in C. teleta utilizing BMP protein and dorsomorphin, and 3) Assess the ancestral role of the BMP antagonist Chordin by analyzing function in C. teleta through CRISPR-Cas9 genome editing and morpholino knockdown. By studying the function of BMP signaling during development of a spiralian annelid, this work will significantly contribute to our understanding of CNS evolution and the involvement of the BMP signaling network in D-V axis specification and CNS formation in the ancestral bilaterian.